HTL/KAI2 signalling substitutes for light to control plant germination

Plants monitor multiple environmental cues, such as light and temperature, to ensure they germinate at the right time and place. Some specialist plants, like ephemeral fire-following weeds and root parasitic plants, germinate primarily in response to small molecules found in specific environments. Although these species come from distinct clades, they use the same HYPOSENSITIVE TO LIGHT/KARRIKIN INSENSITIVE 2 (HTL/KAI2) signalling pathway, to perceive different small molecules suggesting convergent evolution on this pathway. Here, we show that HTL/KAI2 signalling in Arabidopsis thaliana bypasses the light requirement for germination. The HTL/KAI2 downstream component, SUPPRESSOR OF MAX2 1 (SMAX1) accumulates in the dark and is necessary for PHYTOCHROME INTERACTING FACTOR 1/PHYTOCHROME INTERACTING FACTOR 3-LIKE 5 (PIF1/PIL5) to regulate hormone response pathways conducive to germination. The interaction of HTL/KAI2 and light signalling may help to explain how specialist plants like ephemeral and parasitic weeds evolved their germination behaviour in response to specific environments. Specialist plants have convergently evolved to use the same family of receptors to perceive different small molecules in lieu of necessary germination cues, like light. Although light is necessary for the germination of many generalist plants such as the model organism Arabidopsis thaliana, we show that activating the conserved receptor in Arabidopsis promotes germination in the absence of light. We show that the downstream component of the AtKAI2 signalling pathway is stable in the dark which explains its ability to negatively regulate germination. Additionally, we show that activating the receptor in the dark can modulate the gene expression profile by regulating key components of the light signalling pathway. Our study highlights how specialist plants may recycle components of conserved signaling pathways to thrive in new environments.